Domain morphology, boundaries, and topological defects in biophotonic gyroid nanostructures of butterfly wing scales

Singer, Andrej; Boucheron, Leandra; Dietze, Sebastian H.; Jensen, Katharine E.; Vine, David; McNulty, Ian; Dufresne, Eric R.; Prum, Richard O.; Mochrie, Simon G.  J.; Shpyrko, Oleg G.

doi:10.1126/sciadv.1600149

Domain morphology, boundaries, and topological defects in biophotonic gyroid nanostructures of butterfly wing scales

Journal Article · Wed Jun 01 00:00:00 EDT 2016 · Science Advances

DOI:https://doi.org/10.1126/sciadv.1600149· OSTI ID:1625957

Singer, Andrej ^[1]; Boucheron, Leandra ^[2]; Dietze, Sebastian H. ^[2]; Jensen, Katharine E. ^[2]; Vine, David ^[3]; McNulty, Ian ^[4]; Dufresne, Eric R. ^[5]; Prum, Richard O. ^[5]; ^[5]; ^[2]

Univ. of California, San Diego, CA (United States); DOE/OSTI
Univ. of California, San Diego, CA (United States)
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Argonne National Lab. (ANL), Argonne, IL (United States). Center for Nanoscale Materials
Yale Univ., New Haven, CT (United States)

Many organisms in nature have evolved sophisticated cellular mechanisms to produce photonic nanostructures and, in recent years, diverse crystalline symmetries have been identified and related to macroscopic optical properties. However, because we know little about the distributions of domain sizes, the orientations of photonic crystals, and the nature of defects in these structures, we are unable to make the connection between the nanostructure and its development and functionality. We report on nondestructive studies of the morphology of chitinous photonic crystals in butterfly wing scales. Using spatially and angularly resolved x-ray diffraction, we find that the domains are highly oriented with respect to the whole scale, indicating growth from scale boundaries. X-ray coherent diffractive imaging reveals two types of crystalline domain interfaces: abrupt changes between domains emerging from distinct nucleation sites and smooth transitions with edge dislocations presumably resulting from internal stresses during nanostructure development. Our study of the scale structure reveals new aspects of photonic crystal growth in butterfly wings and shows their similarity to block copolymer materials. It opens new avenues to exploration of fundamental processes underlying the growth of biological photonic nanostructures in a variety of species.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of California, San Diego, CA (United States); Yale Univ., New Haven, CT (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-06CH11357; SC0001805; SC0004162

OSTI ID:: 1625957

Journal Information:: Science Advances, Journal Name: Science Advances Journal Issue: 6 Vol. 2; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

Structure of butterfly scales: Patterning in an insect cuticle Ghiradella, Helen Microscopy Research and Technique, Vol. 27, Issue 5 https://doi.org/10.1002/jemt.1070270509	journal	April 1994
The chiral structure of porous chitin within the wing-scales of Callophrys rubi Schröder-Turk, G. E.; Wickham, S.; Averdunk, H. Journal of Structural Biology, Vol. 174, Issue 2 https://doi.org/10.1016/j.jsb.2011.01.004	journal	May 2011
Structural Diversity of Arthropod Biophotonic Nanostructures Spans Amphiphilic Phase-Space Saranathan, Vinodkumar; Seago, Ainsley E.; Sandy, Alec Nano Letters, Vol. 15, Issue 6 https://doi.org/10.1021/acs.nanolett.5b00201	journal	May 2015
Photonic structures in biology Vukusic, Pete; Sambles, J. Roy Nature, Vol. 424, Issue 6950 https://doi.org/10.1038/nature01941	journal	August 2003
Photonic crystals cause active colour change in chameleons Teyssier, Jérémie; Saenko, Suzanne V.; van der Marel, Dirk Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7368	journal	March 2015
Morpho butterfly wing scales demonstrate highly selective vapour response Potyrailo, Radislav A.; Ghiradella, Helen; Vertiatchikh, Alexei Nature Photonics, Vol. 1, Issue 2 https://doi.org/10.1038/nphoton.2007.2	journal	February 2007
Non-polarizing broadband multilayer reflectors in fish Jordan, T. M.; Partridge, J. C.; Roberts, N. W. Nature Photonics, Vol. 6, Issue 11 https://doi.org/10.1038/nphoton.2012.260	journal	October 2012
Weyl points and line nodes in gyroid photonic crystals Lu, Ling; Fu, Liang; Joannopoulos, John D. Nature Photonics, Vol. 7, Issue 4 https://doi.org/10.1038/nphoton.2013.42	journal	March 2013
3D titania photonic crystals replicated from gyroid structures in butterfly wing scales: approaching full band gaps at visible wavelengths Mille, Christian; Tyrode, Eric C.; Corkery, Robert W. RSC Advances, Vol. 3, Issue 9 https://doi.org/10.1039/c2ra22506a	journal	January 2013
Structure, function, and self-assembly of single network gyroid (I4132) photonic crystals in butterfly wing scales Saranathan, V.; Osuji, C. O.; Mochrie, S. G. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 26 https://doi.org/10.1073/pnas.0909616107	journal	June 2010
Sparkling feather reflections of a bird-of-paradise explained by finite-difference time-domain modeling Wilts, B. D.; Michielsen, K.; De Raedt, H. Proceedings of the National Academy of Sciences, Vol. 111, Issue 12 https://doi.org/10.1073/pnas.1323611111	journal	March 2014
VII. On the optical character of some brilliant animal colours Rayleigh, Lord The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science, Vol. 37, Issue 217 https://doi.org/10.1080/14786440108635867	journal	January 1919
Iridescence and spectral filtering of the gyroid-type photonic crystals in Parides sesostris wing scales Wilts, Bodo D.; Michielsen, Kristel; De Raedt, Hans Interface Focus, Vol. 2, Issue 5 https://doi.org/10.1098/rsfs.2011.0082	journal	December 2011
Gyroid cuticular structures in butterfly wing scales: biological photonic crystals Michielsen, K.; Stavenga, D. G. Journal of The Royal Society Interface, Vol. 5, Issue 18 https://doi.org/10.1098/rsif.2007.1065	journal	June 2007
Alignment of crystal orientations of the multi-domain photonic crystals in Parides sesostris wing scales Yoshioka, S.; Fujita, H.; Kinoshita, S. Journal of The Royal Society Interface, Vol. 11, Issue 92 https://doi.org/10.1098/rsif.2013.1029	journal	March 2014
Quantified interference and diffraction in single Morpho butterfly scales Vukusic, P.; Sambles, J. R.; Lawrence, C. R. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 266, Issue 1427 https://doi.org/10.1098/rspb.1999.0794	journal	July 1999
A review of the diversity and evolution of photonic structures in butterflies, incorporating the work of John Huxley (The Natural History Museum, London from 1961 to 1990) Ingram, A. L.; Parker, A. R. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1502 https://doi.org/10.1098/rstb.2007.2258	journal	January 2007
Water window ptychographic imaging with characterized coherent X-rays Rose, Max; Skopintsev, Petr; Dzhigaev, Dmitry Acta Crystallographica Section A Foundations and Advances, Vol. 71, Issue a1 https://doi.org/10.1107/s2053273315097739	journal	August 2015
High-Resolution Scanning X-ray Diffraction Microscopy Thibault, P.; Dierolf, M.; Menzel, A. Science, Vol. 321, Issue 5887 https://doi.org/10.1126/science.1158573	journal	July 2008
Sculpted-multilayer optical effects in two species of Papilio butterfly Vukusic, Peter; Sambles, Roy; Lawrence, Christopher Applied Optics, Vol. 40, Issue 7 https://doi.org/10.1364/ao.40.001116	journal	January 2001
Coherent x-ray imaging of defects in colloidal crystals Gulden, J.; Yefanov, O. M.; Mancuso, Adrian Paul Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/phppubdb-16314	text	January 2010
Development of butterfly scales. II. Struts, lattices and surface tension: BUTTERFLY SCALE DEVELOPMENT Ghiradella, H.; Radigan, W. Journal of Morphology, Vol. 150, Issue 2 https://doi.org/10.1002/jmor.1051500202	journal	October 1976
Beyond butterflies—the diversity of biological photonic crystals Welch, V. L.; Vigneron, J. -P. Optical and Quantum Electronics, Vol. 39, Issue 4-6 https://doi.org/10.1007/s11082-007-9094-4	journal	July 2007
Quantitative measurement of displacement and strain fields from HREM micrographs Hÿtch, M. J.; Snoeck, E.; Kilaas, R. Ultramicroscopy, Vol. 74, Issue 3, p. 131-146 https://doi.org/10.1016/S0304-3991(98)00035-7	journal	August 1998
Electron tomography and computer visualisation of a three-dimensional ‘photonic’ crystal in a butterfly wing-scale Argyros, A.; Manos, S.; Large, M. C. J. Micron, Vol. 33, Issue 5 https://doi.org/10.1016/S0968-4328(01)00044-0	journal	January 2002
Patterning with block copolymer thin films Segalman, Rachel A. Materials Science and Engineering: R: Reports, Vol. 48, Issue 6, p. 191-226 https://doi.org/10.1016/j.mser.2004.12.003	journal	February 2005
Controlled Replication of Butterfly Wings for Achieving Tunable Photonic Properties Huang, Jingyun; Wang, Xudong; Wang, Zhong Lin Nano Letters, Vol. 6, Issue 10 https://doi.org/10.1021/nl061851t	journal	October 2006
Aphrodite's iridescence Parker, Andrew R.; McPhedran, Ross C.; McKenzie, David R. Nature, Vol. 409, Issue 6816 https://doi.org/10.1038/35051168	journal	January 2001
Transport and Anderson localization in disordered two-dimensional photonic lattices Schwartz, Tal; Bartal, Guy; Fishman, Shmuel Nature, Vol. 446, Issue 7131 https://doi.org/10.1038/nature05623	journal	March 2007
A beamline for 1–4 keV microscopy and coherence experiments at the Advanced Photon Source McNulty, I.; Khounsary, A.; Feng, Y. P. Review of Scientific Instruments, Vol. 67, Issue 9 https://doi.org/10.1063/1.1147339	journal	September 1996
Solid State Physics Ashcroft, N. W.; Mermin, N. D.; Smoluchowski, R. Physics Today, Vol. 30, Issue 1 https://doi.org/10.1063/1.3037370	journal	January 1977
Disordered animal multilayer reflectors and the localization of light Jordan, T. M.; Partridge, J. C.; Roberts, N. W. Journal of The Royal Society Interface, Vol. 11, Issue 101 https://doi.org/10.1098/rsif.2014.0948	journal	December 2014
Coherent x-ray imaging of defects in colloidal crystals Gulden, J.; Yefanov, O. M.; Mancuso, A. P. Physical Review B, Vol. 81, Issue 22 https://doi.org/10.1103/PhysRevB.81.224105	journal	June 2010
Circular Dichroism in Biological Photonic Crystals and Cubic Chiral Nets Saba, M.; Thiel, M.; Turner, M. D. Physical Review Letters, Vol. 106, Issue 10 https://doi.org/10.1103/PhysRevLett.106.103902	journal	March 2011
Hard-X-Ray Lensless Imaging of Extended Objects Rodenburg, J. M.; Hurst, A. C.; Cullis, A. G. Physical Review Letters, Vol. 98, Issue 3 https://doi.org/10.1103/PhysRevLett.98.034801	journal	January 2007
Diffraction-limited storage rings – a window to the science of tomorrow Eriksson, Mikael; van der Veen, J. Friso; Quitmann, Christoph Journal of Synchrotron Radiation, Vol. 21, Issue 5 https://doi.org/10.1107/S1600577514019286	journal	August 2014
Water window ptychographic imaging with characterized coherent X-rays Rose, Max; Skopintsev, Petr; Dzhigaev, Dmitry Journal of Synchrotron Radiation, Vol. 22, Issue 3 https://doi.org/10.1107/S1600577515005524	journal	April 2015
Cavity Quantum Electrodynamics with Anderson-Localized Modes Sapienza, L.; Thyrrestrup, H.; Stobbe, S. Science, Vol. 327, Issue 5971 https://doi.org/10.1126/science.1185080	journal	March 2010
optix Drives the Repeated Convergent Evolution of Butterfly Wing Pattern Mimicry Reed, R. D.; Papa, R.; Martin, A. Science, Vol. 333, Issue 6046 https://doi.org/10.1126/science.1208227	journal	July 2011
Switchable Static and Dynamic Self-Assembly of Magnetic Droplets on Superhydrophobic Surfaces Timonen, J. V. I.; Latikka, M.; Leibler, L. Science, Vol. 341, Issue 6143 https://doi.org/10.1126/science.1233775	journal	July 2013
Grain Growth in Thin Films Thompson, C. V. Annual Review of Materials Science, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.ms.20.080190.001333	journal	August 1990
Sculpted-multilayer optical effects in two species of Papilio butterfly Vukusic, Peter; Sambles, Roy; Lawrence, Christopher Applied Optics, Vol. 40, Issue 7 https://doi.org/10.1364/AO.40.001116	journal	January 2001
Defect modes of a two-dimensional photonic crystal in an optically thin dielectric slab Painter, O.; Vučkovič, J.; Scherer, A. Journal of the Optical Society of America B, Vol. 16, Issue 2 https://doi.org/10.1364/JOSAB.16.000275	journal	January 1999
Observations of artefacts in the x-ray ptychography method Burdet, Nicolas; Morrison, Graeme R.; Huang, Xiaojing Optics Express, Vol. 22, Issue 9 https://doi.org/10.1364/OE.22.010294	journal	January 2014

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Cuticle network and orientation preference of photonic crystals in the scales of the weevil Lamprocyphus augustus Ebihara, R.; Hashimoto, H.; Kano, J. Journal of The Royal Society Interface, Vol. 15, Issue 145 https://doi.org/10.1098/rsif.2018.0360	journal	August 2018
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Ptychographic X-ray computed tomography at a high-brilliance X-ray source Sala, Simone; Batey, Darren J.; Prakash, Anupama Optics Express, Vol. 27, Issue 2 https://doi.org/10.1364/oe.27.000533	journal	January 2019

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